25 States recovered salmonellae from 65 per cent of samples taken from moderately polluted streams, 38 per cent from minimally polluted and 44 per cent from unpolluted. The persistence of Salmonella organisms in shell-fish is a well recognized public health problem, but experimentally it has also been demonstrated that S. enteritidis will persist in the intestine of tench 60 days and the gut of carp 68 days after a single infected feed, the isolates recovered showing no loss of pathogenicity for mice. SUMMARY IN Britain the veterinary authorities through the Zoonoses Order and proposed Protein Processing Legislation are now taking positive steps to collect data on the incidence and trends of salmonellosis. This legislation will also have an impact at certain points in the Salmonella cycle. In formulating this legislation due regard has been given to the advances made by workers abroad, but we must continually remain aware of research and development elsewhere and seek to exchange information on all aspects of the problem. May I suggest that serious consideration should urgently be given to those areas outlined in this paper where other countries have recognized a problem and are actively engaged in research and control measures. These are: (1) Improvements in imported and home produced animal protein feedstuffs to reduce the level of Salmonella contamination, (2) Pelleting of animal feedstuffs, (3) A reduction in the potential hazards from slaughtered livestock by (a) Routine ante-mortem inspection; (b) Separate slaughter of casualties; (c) Bacteriological examination of all casualties and animals from known Salmonella infected herds; and (d) Specific criteria for the judgement of carcass and offal on the basis of laboratory results. .
(4) Water pollution particularly from human sewage effluent. (5)The possible infection of freshwater fish and persistence in fish. (6) The role of wildlife as a reservoir of Salmonellas. (7) The possible control and eradication of S. dublin infection. Most if not all of these measures require active collaboration between veterinary, medical, and environmental health authorities. In particular I suggest that the present standards prevailing in meat hygiene could be greatly improved with a consequent reduction in the public health risks from Salmonellosis.
REFERENCES 1 Public Health Service Laboratory Working Group. SKOVGAARD, N. and NEILSEN. BB (1972) J. Hyg. Camb. 70 , 127. EDEL- W, (1974) Thesis. Comparative Studies on Salmonella 2 Isolation. Utrecht Thesis. 3 SCHOTHORST M. VAN, LEUSDEN F. M. VAN, EDEL W. and KAMPELMACHER, E. H. (1974) Tijdschr. Diergeneesk 99, 815. 4 DIJKSTRA, R. G. (1973) Vet. Rec. 93, 467. 5 KAMPELMACHER, E.H. and JANSEN, L. M. VAN (1973) Zent bl Bakt ParasitKde I Abt Orig B, 157, 71. 6 EDFL W. SCHOTHORST M. VAN GUINEE, P. A. M. and KAMPELMACHER, E. H. (1974) Zent bl Bakt ParasitKde I. Abt Orig A., 226, 314. 7 VOETEN, A. C., BRUS, D. H. J. and JAARTSVELD, F. H. J. (1974) Tijdschr Diergeneesk, 99, 1093. 8 EDEL, W. (1974) Thesis. Comparative Studies on Salmonella Isolation. Utrecht Thesis. 9 OSTLUND, K (1973). 6th International Symposium W.A.V.F.H. Elsinore Denmark 1973. 10 HURVEIL, B, BORG, K., GUNNARSSON, A. and JERRING, J. (1973) XIth Int. Congr. of Game Biologists Stockholm. Sept. 3-7, pp. 493. 11 POHN, H. P. (1975) Bundesgesundheitsblatt, 18 ,53. 12 PIETZSCH, O. (1975) Personal communication. 13 HESS, E., LOTT, G. and BREER, C. (1974) Zent bl Bakt ParasitK de I Abt Orig B., 158, 446. 14 PAGON, S., SONNABEND, W. and KRECH, U. (1974) Zent bl Bakt ParasitKde I Abt Orig B., 158, 394. 15 CHERRY, W. B., HANKS, J. B., THOMASON, B. M., MURLIN, A. M., BIDDLE, J. W. and CROON, J. M. (1972) Appl Microbiol, 24, 334.
(c) SALMONELLA INFECTIONS OF MAN DERIVED FROM ANIMALS
J. H.
McCOY,
Public Health
M.B., D.P.H.
Laboratory
Service
RGANISMS of the Salmonella group are distributed in nature. With the excepof fish, aquatic mammals and animals living in unpolluted waters, salmonellae have been isolated from all species of domesticated and wild animals and birds, and from reptiles. Some 1700 serotypes differentiated by antigenic analysis have now been recognized, each one of which is capable of causing disease in animals or man or in both when ingested in sufficient numbers.
tion
~ widely
On epidemiological grounds, a few serotypes are classed as host adapted, that is producing disease in the host species, only rarely in other species. Examples are Salmonella typhi and S. paratyphi A, B, and C, which cause enteric fevers in man, but which do not cause disease in any other animal species; S. dublin, the cause of serious disease in cattle; S. cholerae-suis in pigs; S. gallinarum and S. pullorum in fowl; and S. abortus-ovis in sheep. Other serotypes, though not host adapted, may
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26 TABLEI
Clinical Animal and Human Salmonellosis. 1958-67
TABLE II Clinical Animal & Human Salmonellosis. 1958-67 18 serotypes most commonly isolated from humans. (percentages in parentheses)
through methods of animal husbandry and in particular by methods of intensive animal production become associated for longer or shorter periods with particular species of domestic animals or fowl. In the U.S.A. for many years domestic fowl have formed the largest reservoir from which salmonellae were transmitted to humans: in Germany and Holland pigs: in the United Kingdom cattle. The host-adapted serotypes are responsible for serious illness characterized by invasion of the blood stream with high morbidity and mortality. A proportion of those infected become chronic carriers, harbouring the organism within the body and excreting it in faeces for the rest of their life. Other serotypes produce a less serious illness characterized by intestinal symptoms of short duration with low mortality. Chronic carriers are rare, but symptomless infection and excretion are common. In the majority of those infected excretion of
TABLE III Salmonella isolated from normal animals slaughter 1961-62 (percentage in parentheses)
at
the organism occurs during the active stages of illness and for some weeks after recovery. Invasion of the blood stream is rare. Table I shows the incidence of infection in animals and man by host-adapted and host-associated serotypes during the period 1957-68 ’2. Host-adapted serotypes were isolated from 71 per cent (of animal) and from 1 per cent of human infections: host associated serotypes from 26 per cent of animal infections but from 58 per cent of human infections. Table II shows human infections caused by eighteen serotypes, other than those in Table I, most frequently isolated from humans during this period and their isolations from animal sources. These serotypes were isolated from 19 per cent of human infections but from only 1 ~ 5 per cent of animal infections. So far we have considered clinical infections in animals. We should now consider normal healthy animals and for this purpose the results of a survey of abattoirs in 1961/62 are available 3. During this period sewer swabs were examined weekly from thirty-two abattoirs in England and Wales. Table III shows that with the
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27
exception
of S. dublin in cattle and
pigs
host
TABLE IV
adapted
serotypes were rarely isolated from healthy animals. S. typhi-murium, however, was isolated from approximately 25 per cent of specimens from all types of abat-
Salmonellae isolated from normal animals
at
slaughter
1961-62
toirs. The isolation of S. paratyphi B, a host adapted serotype of man, from general abattoirs and in particular from an abattoir slaughtering aged dairy cows is of particular interest in view of the association of human infection with contaminated milk. Table IV shows isolations of eighteen other serotypes most commonly isolated from human infections excluding host adapted and host associated serotypes. Comparison with Table II shows that while these serotypes were isolated from 93 out of 10,640 (< 1 per cent) clinical infections in cattle, pigs and sheep, isolations of these serotypes from abattoirs slaughtering healthy cattle, pigs and sheep amounted to 30 per cent (365 out of 1,203 isolations).
CLINICAL INFECTION AND SYMPTOMLESS EXCRETION HUMAN and animal feeding experiments have shown that in general the numbers of salmonellae ingested determine the occurrence of clinical illness. Human volunteer experiments on healthy adult males in the U.S.A. 456with serotypes isolated from dried egg showed that doses of approximately 150,000 of S. anatum and S. meleagridis orgaiiisms failed to produce clinical symptoms in volunteers but that symptomless excretion could be demonstrated in approximately 50 per cent. (Table V). Increasing the dose of organisms to about five millions produced clinical infection in 11I per cent, symptomless excretion in 74 per cent of volunteers. With doses of 50-67 millions of organisms clinical illness was produced in 32 per cent, symptomless excretion in 65 per cent of subjects. With S. pullorum, a host adapted serotype of fowl, doses of 16,000 million organisms were required to produce transient illness and excretion in volunteers. The point well illustrated in these experiments is the relationship of clinical illness to the number of organisms ingested. In outbreaks the number of symptomless excretors may be expected to equal or exceed the number of clinical illnesses. Indeed large numbers of excretors may be found in the absence of clinical illness. These findings in man are generally applicable to animals. Smith7 (1960) showed that pigs fed on food naturally contaminated with salmonellae excreted saulmonellae in their faeces from time to time in the absence of clinical illness but that salmonellae were not isolated after use of the contaminated food ceased. Gordon and Tucker8 (1965) fed food artificially contaminated with S. menston to salmonella-free chicks and demonstrated a cycle of infection in that S. menston was shown to be present in the adult fowl, the eggs laid by these fowl, the chicks hatched from these eggs and the eggs laid by these progeny at maturity. Infection of water supplies was shown to be an additional source of infection for the chicks. The finding that infection of the environment was an important method for the transmission of infection extended to fowl the observations made by McDonagh and Smith9 (1958) on the transfer of infection between pigs held at abattoirs for extended periods. The significance of the healthy animal or fowl excreting salmonella is that during slaughter contamination of the surfaces of carcases with intestinal contents is unavoidable.
TABLE V Human volunteer experiments (percentages in parentheses)
HUMAN SALMONELLOSIS THE PERIOD examined is from 1940 to 1973, for which years human salmonellosis is adequately documented in the Annual Reports of Food Poisoning of the P.H.L.S.2 ’0 &dquo; Figure 1 shows the trends of human infections with S. typhi-murium and with serotypes other than S. typhi-murium during the period. In general three main trends can be distinguished. 1939-55. During this period human food and animal feed was rationed and infections were reduced to a minimum. As milk was regarded as a most important human food the greater part of imported animal feed was allocated to dairy cattle. Pig and poultry populations received only the amount necessary to maintain breeding herds and flocks. The fall in egg production was made up by the import of spray-dried egg from the U.S.A. and other countries for which contracts for production had been negotiated before the War. The control of meat supplies was effected by a reduction in the number of abattoirs from a pre-War figure of about 15,000 to 500 whose production was controlled. The restriction of cattle feed resulted in the slaughter of almost all the male calves produced by the dairy herd, in number 1 to 1.5 million annually. The concentration of animals at collecting centres and abattoirs during this period offered opportunity for the transfer of salmonella infection with consequent contamination of carcase meats with salmonellae from gut contents during slaughter. During this period, canned meats formed part of the meat ration and
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28 canned and
raw
meats were
commonly
delivered
together by retailers, affording opportunity of contaminormally eaten without further cooking, by carcase meats. In the period 1923-39 only fourteen salmonella nation of canned meats,
serotypes had been isolated from human infections in
and Wales. Spray-dried egg introduced another thirty-four serotypes which appeared in both human and pig populations as material unfit for human consumption was used to supplement supplies of animal feed. The import of spray-dried egg from the U.S.A. ceased with the abrupt ending of Lease-Lend in 1947, and imports of frozen liquid egg were obtained from ’soft currency’ arenas mainly within the Commonwealth. Some liquid egg was home-produced, mainly from cracked eggs at packing stations. Liquid egg introduced further serotypes from 1947 until 1964 when pasteurization of liquid egg became compulsory. Extensive surveys of liquid egg in the mid-1950s showed that Chinese liquid egg and egg products were heavily contaminated with S. paratyphi B and that homeproduced liquid egg was heavily contaminated with S. typhi-murium. The main vehicles through which these serotypes were conveyed to the population were sweetmeats and bakers’ confectionery, as liquid egg was used raw in the production of artificial creams. The ending of the rationing of human food and animal feed in 1953 led paradoxically to an immediate rise in human infection: the result of the distribution of food stocks accumulated by the Ministry of Food and of the return of abattoirs to private hands. The number of abattoirs increased in a relatively short period from 500 controlled abattoirs to about 5,000 private abattoirs where the shortage of experienced slaughtermen and meat inspectors was evident.
England
FIGURE 1. Incidents
of human
salmonella
infection England and Wales
After the hot summer of 1959 however, a general fall in infections with S. typhi-murium became apparent. This trend continued to 1965, after which year the annual incidence of S. typhi-murium infection became stabilized. This fall was the result of many factors of which the limitation of production of liquid egg to licensed plants, the introduction of pasteurization by the British Egg Marketing Board after its formation in 1957 and the growth of calf rearing which reduced to a minimum the number of day-old calves sent for slaughter are probably the most important. The marked increase in the number of infections with serotypes other than S. typhi-murium which occurred after the cessation of rationing may be attributed to the rapid reconstitution of the pig and poultry industries from the breeding stocks maintained during the period of rationing. With the import of animal and marine protein (meat and bone meals, fish meals) heavily contaminated with salmonella (notably Angolan sun-dried fish meal) many serotypes were introduced not only to England and Wales but to Europe at large. Once introduced many serotypes persisted, being recycled to animals through the conversion of inedible offals into animal feed. The most important factor in the increase of human infections due to other serotypes was the reconstitution of the poultry industry, both egg producing and broiler producing, which was remade on intensive lines in which a small number of specialist breeders supplied millions of day-old chicks to rearing farms. The cycle of transmission from the introduction of infection into a breeding flock has already been describedg and transmission of infection to man by raw egg products or by poultry meat can continue for many years without the necessity for continued introductions. By the end of the 1950s frozen eviscerated broiler
resulting
1942-73
3-year moving average.
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29 had replaced chilled uneviscerated poultry and had allowed expansion of the industry to proceed at so rapid a rate that by 1964, frozen poultry meat had become the cheapest flesh food available. Consumption of poultry meat increased so that by the 1970s, the annual consumption per head of poultry meat exceeded that of lamb and mutton and equalled consumption of pork. From 1963 onwards the import of fertile eggs for hatching and of day-old chicks was resumed to introduce desirable genes into native poultry breeding stocks. This led to the associated importation of salmonella serotypes, notably S. infantis, S. heidelberg, S. montevideo, S. indiana, and S. enteritidis, which became rapidly established in breeding flocks with egg transmission to offspring. Two serotypes, Salmonella unidentified 4, 12:d:-, and S. agona were introduced into poultry, pig and cattle herds through contaminated imported fish meals towards the end of the 1960s.
TABLE VI
carcases carcases
Human Salmonellosis Vehicles of infection. General and family outbreaks.
TABLE VII Human Salmonellosis Meat vehicles. General and family outbreaks.
&dquo;
VEHICLES OF INFECTION TABLE VI shows the foods involved in general and family outbreaks for which information was available. These outbreaks, 1,032 over the entire period, represent about 9 per cent of the 11,539 outbreaks reported. The trends of interest are the increasing proportion of outbreaks attributed to meat and milk, and the decreasing proportion attributed to sweetmeats which include bakers’ confectionery, and eggs. This latter trend can be attributed to the decrease in consumption of duck eggs which during food rationing were unrationed and the introduction of pasteurization for
TABLE VIII Human Salmonellosis. England and Wales Location of Outbreaks.
liquid
egg. The milk outbreaks were generally attributed to the consumption of raw milk which is currently supplied by about 6,000 producer retailers and represents about 3 per cent of milk consumption. Many of these outbreaks occurred in the families of milk producers where cows were infected with S. dublin or S. typhi-murium. The remainder were extensive outbreaks occurring in institutions, holiday camps and hotels supplied with raw milk. In a proportion of these latter outbreaks, symptomless excretion of the serotype responsible was demonstrated in the herds involved. Table VII shows general trends in the type of meats involved in general and family outbreaks. Two main trends are apparent: an increase in outbreaks attributed to poultry; a decrease in those attributable to made-up meats. During the period of food rationing and immediately afterwards made-up meats were involved in approximately 30 per cent of outbreaks. Readycooked meats (roast beef, pork, boiled ham) prepared centrally and distributed to retailers over wide areas have been increasingly identified as vehicles of infection. In the outbreaks recorded, undercooking or post-cooking contamination has been common. This problem results from the shrinkage of flesh meats on cooking, and a fine balance has to be struck empirically between adequate cooking and minimum shrinkage. Poultry outbreaks have been generally associated with spit-roasted poultry and turkey outbreaks associated with large (20-25 lb) ’banqueting’ birds. Most of these latter outbreaks have been associated with inadequate cooking, inadequate cooling, or postcooking contamination of sliced meats. Table VIII shows the trends in the locations where outbreaks have occurred. Throughout the period considered roughly 50 per cent of outbreaks of salmonellosis reported have occurred in hospitals.
Outbreaks
however,
are, occurring in hospitals andtoinstitutions likely to be brought attention more
more
rapidly and to be more thoroughly investigated and reported than outbreaks in other locations. Much the same consideration applies to canteen and institutional outbreaks, which share with hospitals a known population easily accessible for investigation of outbreaks. In hospitals, particularly children’s hospitals, maternity hospital nurseries, and geriatric hospitals and wards, outbreaks, not food-borne, often originate from the admission of an undiagnosed case of salmonellosis or symptomless excretor of salmonella, from whom infection is transmitted by direct or indirect contact. In some of such hospital outbreaks, infections have occurred for many weeks or even months. Experience suggests that about 50 per cent of hospital outbreaks fall into this category.
Hotel outbreaks occurred at more or less the same level until the period 1969/72, when outbreaks doubled. This increase can be associated with dinners and receptions at which the large ’banqueting’ birds previously mentioned were served. Table IX shows the change in rank order of the ten serotypes most frequently isolated from human infections over the period. Of the serotypes isolated in England and Wales up to 1939, three, S. typhi-murium, S. enteritidis, and S. stanley hold their original position. S. thompson, egg transmitted in laying flocks, ceased to be of major
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30
rationing in
TABLE IX
Salmonellosis.
England
1953. S.
brandenburg was introduced in the
same manner.
and Wales
S. virchow was associated with spit-roasted poultry since an extensive outbreak from this source in 1968. S. agona has been associated with meat, milk and poultry products since its introduction in imported fish meal.
Rank order of the top 10 serotypes
REFERENCES
1 SOJKA, W. J. and FIELD, H. I. (1970) "Salmonellosis in England and Wales 1958-1967." Veterinary Bulletin, 40, 515. 2 PHLS reports. "Food Poisoning in England and Wales. Annual reports 1958-1967." Monthly Bulletin of the Ministry of Health and the Public Health
Laboratory Service
1959-1967. Public
Health, London (1969) 83, 205.
3 Report (1964). "Salmonellae in abattoirs, butcher shops, and home-produced meat, and their relation to human infection." Journal
4
5
6
7
of Hygiene, 62,
283.
N. B. and EISELE, C. W. (1951a). "Experimental Human Salmonellosis. I." Journal of Infectious Diseases, 88, 278. McCULLOUGH, N. B. and EISELE, C. W. (1951b). "Experimental Human Salmonellosis. III ." Journal of Infectious Diseases, 89 , 209. McCULLOUGH, N. B. and EISELE, C. W. "Experimental Human Salmonellosis. IV." Journal of Infectious Diseases, 89, 259. SMITH, H. WILLIAMS (1960). "The effect of feeding pigs on food
McCuLLOUGH,
naturally contaminated with Salmonellae."Journal of Hygiene, 58,
381. R. F. and TUCKER, J. F. (1965). "The epizootology of Salmonella Menston infection of fowl and the effect of feeding poultry food artificially infected with salmonella." British Poultry Science, 6, 251. 9 McDONAGH, V. P. and SMITH, H. G. (1958). "The Significance of the Abattoir in Salmonella infection in Bradford." Journal of Hygiene, 56, 271. Reports (1970). "Food Poisoning and Salmonella infections in 10 England and Wales. 1968." Public Health, London, 84, 239. 11 Reports (1974). "Food Poisoning and Salmonella infections in . 225 England and Wales. 1969-1972." Public Health, London, 88,
8 GORDON,
importance after the introduction of pasteurization of liquid egg in 1964, though a small number of infections with this serotype still occur. S. meleagridis, S. oranienburg, S. montevideo, and S. anatum, were introduced by imported spray-dried hen egg during the period of rationing, and were later introduced to flocks and herds by imported protein constituents of animal feed after the cessation of
SALMONELLA INFECTIONS IN ANIMALS AND BIRDS
A. D. OSBORNE, M.R.C.V.S., D.V.S.M., M.R.C.PATH,
Senior Lecturer in
Veterinary Public Health, University of Bristol
the first identification of a specific orassociated with disease in pigs, which was the name Bacillus cholerae-suis by Salmon in 1885, the widespread implication of similar organisms with disease processes in animals of almost every species has been demonstrated. Although by no means absolute it is possible to make a distinction between those members of the group which are primarily involved with disease in a single host (e.g. Salmonella typhi in man S. abortus ovis in sheep, S. pullorum in poultry) and those which are associated with disease, or occasionally found as little more than commensals, in a wide variety of animal species (e.g. S. typhimurium, S.
INCE
ganism given
F.R.S.H.
newport).
It is the latter group with which this paper is concerned in the main, since the Zoonoses Order is obviously designed to improve the possibilities of control of spread of such agents. In consideration of hosts of such salmonella, those from which humans are most likely to derive infection must be our primary concern, but opportunity will be taken to indicate some of the less common possible sources of infection for man.
In considering diseases associated with infection by members of this large group of organisms, it is salutary to realize that the incidence of infection has decreased
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(4) Water pollution particularly from human sewage effluent. (5)The possible infection of freshwater fish and persistence in fish. (6) The role of wildlife as a reservoir of Salmonellas. (7) The possible control and eradication of S. dublin infection. Most if not all of these measures require active collaboration between veterinary, medical, and environmental health authorities. In particular I suggest that the present standards prevailing in meat hygiene could be greatly improved with a consequent reduction in the public health risks from Salmonellosis.
REFERENCES 1 Public Health Service Laboratory Working Group. SKOVGAARD, N. and NEILSEN. BB (1972) J. Hyg. Camb. 70 , 127. EDEL- W, (1974) Thesis. Comparative Studies on Salmonella 2 Isolation. Utrecht Thesis. 3 SCHOTHORST M. VAN, LEUSDEN F. M. VAN, EDEL W. and KAMPELMACHER, E. H. (1974) Tijdschr. Diergeneesk 99, 815. 4 DIJKSTRA, R. G. (1973) Vet. Rec. 93, 467. 5 KAMPELMACHER, E.H. and JANSEN, L. M. VAN (1973) Zent bl Bakt ParasitKde I Abt Orig B, 157, 71. 6 EDFL W. SCHOTHORST M. VAN GUINEE, P. A. M. and KAMPELMACHER, E. H. (1974) Zent bl Bakt ParasitKde I. Abt Orig A., 226, 314. 7 VOETEN, A. C., BRUS, D. H. J. and JAARTSVELD, F. H. J. (1974) Tijdschr Diergeneesk, 99, 1093. 8 EDEL, W. (1974) Thesis. Comparative Studies on Salmonella Isolation. Utrecht Thesis. 9 OSTLUND, K (1973). 6th International Symposium W.A.V.F.H. Elsinore Denmark 1973. 10 HURVEIL, B, BORG, K., GUNNARSSON, A. and JERRING, J. (1973) XIth Int. Congr. of Game Biologists Stockholm. Sept. 3-7, pp. 493. 11 POHN, H. P. (1975) Bundesgesundheitsblatt, 18 ,53. 12 PIETZSCH, O. (1975) Personal communication. 13 HESS, E., LOTT, G. and BREER, C. (1974) Zent bl Bakt ParasitK de I Abt Orig B., 158, 446. 14 PAGON, S., SONNABEND, W. and KRECH, U. (1974) Zent bl Bakt ParasitKde I Abt Orig B., 158, 394. 15 CHERRY, W. B., HANKS, J. B., THOMASON, B. M., MURLIN, A. M., BIDDLE, J. W. and CROON, J. M. (1972) Appl Microbiol, 24, 334.
(c) SALMONELLA INFECTIONS OF MAN DERIVED FROM ANIMALS
J. H.
McCOY,
Public Health
M.B., D.P.H.
Laboratory
Service
RGANISMS of the Salmonella group are distributed in nature. With the excepof fish, aquatic mammals and animals living in unpolluted waters, salmonellae have been isolated from all species of domesticated and wild animals and birds, and from reptiles. Some 1700 serotypes differentiated by antigenic analysis have now been recognized, each one of which is capable of causing disease in animals or man or in both when ingested in sufficient numbers.
tion
~ widely
On epidemiological grounds, a few serotypes are classed as host adapted, that is producing disease in the host species, only rarely in other species. Examples are Salmonella typhi and S. paratyphi A, B, and C, which cause enteric fevers in man, but which do not cause disease in any other animal species; S. dublin, the cause of serious disease in cattle; S. cholerae-suis in pigs; S. gallinarum and S. pullorum in fowl; and S. abortus-ovis in sheep. Other serotypes, though not host adapted, may
Downloaded from rsh.sagepub.com at UCSF LIBRARY & CKM on March 18, 2015
26 TABLEI
Clinical Animal and Human Salmonellosis. 1958-67
TABLE II Clinical Animal & Human Salmonellosis. 1958-67 18 serotypes most commonly isolated from humans. (percentages in parentheses)
through methods of animal husbandry and in particular by methods of intensive animal production become associated for longer or shorter periods with particular species of domestic animals or fowl. In the U.S.A. for many years domestic fowl have formed the largest reservoir from which salmonellae were transmitted to humans: in Germany and Holland pigs: in the United Kingdom cattle. The host-adapted serotypes are responsible for serious illness characterized by invasion of the blood stream with high morbidity and mortality. A proportion of those infected become chronic carriers, harbouring the organism within the body and excreting it in faeces for the rest of their life. Other serotypes produce a less serious illness characterized by intestinal symptoms of short duration with low mortality. Chronic carriers are rare, but symptomless infection and excretion are common. In the majority of those infected excretion of
TABLE III Salmonella isolated from normal animals slaughter 1961-62 (percentage in parentheses)
at
the organism occurs during the active stages of illness and for some weeks after recovery. Invasion of the blood stream is rare. Table I shows the incidence of infection in animals and man by host-adapted and host-associated serotypes during the period 1957-68 ’2. Host-adapted serotypes were isolated from 71 per cent (of animal) and from 1 per cent of human infections: host associated serotypes from 26 per cent of animal infections but from 58 per cent of human infections. Table II shows human infections caused by eighteen serotypes, other than those in Table I, most frequently isolated from humans during this period and their isolations from animal sources. These serotypes were isolated from 19 per cent of human infections but from only 1 ~ 5 per cent of animal infections. So far we have considered clinical infections in animals. We should now consider normal healthy animals and for this purpose the results of a survey of abattoirs in 1961/62 are available 3. During this period sewer swabs were examined weekly from thirty-two abattoirs in England and Wales. Table III shows that with the
Downloaded from rsh.sagepub.com at UCSF LIBRARY & CKM on March 18, 2015
27
exception
of S. dublin in cattle and
pigs
host
TABLE IV
adapted
serotypes were rarely isolated from healthy animals. S. typhi-murium, however, was isolated from approximately 25 per cent of specimens from all types of abat-
Salmonellae isolated from normal animals
at
slaughter
1961-62
toirs. The isolation of S. paratyphi B, a host adapted serotype of man, from general abattoirs and in particular from an abattoir slaughtering aged dairy cows is of particular interest in view of the association of human infection with contaminated milk. Table IV shows isolations of eighteen other serotypes most commonly isolated from human infections excluding host adapted and host associated serotypes. Comparison with Table II shows that while these serotypes were isolated from 93 out of 10,640 (< 1 per cent) clinical infections in cattle, pigs and sheep, isolations of these serotypes from abattoirs slaughtering healthy cattle, pigs and sheep amounted to 30 per cent (365 out of 1,203 isolations).
CLINICAL INFECTION AND SYMPTOMLESS EXCRETION HUMAN and animal feeding experiments have shown that in general the numbers of salmonellae ingested determine the occurrence of clinical illness. Human volunteer experiments on healthy adult males in the U.S.A. 456with serotypes isolated from dried egg showed that doses of approximately 150,000 of S. anatum and S. meleagridis orgaiiisms failed to produce clinical symptoms in volunteers but that symptomless excretion could be demonstrated in approximately 50 per cent. (Table V). Increasing the dose of organisms to about five millions produced clinical infection in 11I per cent, symptomless excretion in 74 per cent of volunteers. With doses of 50-67 millions of organisms clinical illness was produced in 32 per cent, symptomless excretion in 65 per cent of subjects. With S. pullorum, a host adapted serotype of fowl, doses of 16,000 million organisms were required to produce transient illness and excretion in volunteers. The point well illustrated in these experiments is the relationship of clinical illness to the number of organisms ingested. In outbreaks the number of symptomless excretors may be expected to equal or exceed the number of clinical illnesses. Indeed large numbers of excretors may be found in the absence of clinical illness. These findings in man are generally applicable to animals. Smith7 (1960) showed that pigs fed on food naturally contaminated with salmonellae excreted saulmonellae in their faeces from time to time in the absence of clinical illness but that salmonellae were not isolated after use of the contaminated food ceased. Gordon and Tucker8 (1965) fed food artificially contaminated with S. menston to salmonella-free chicks and demonstrated a cycle of infection in that S. menston was shown to be present in the adult fowl, the eggs laid by these fowl, the chicks hatched from these eggs and the eggs laid by these progeny at maturity. Infection of water supplies was shown to be an additional source of infection for the chicks. The finding that infection of the environment was an important method for the transmission of infection extended to fowl the observations made by McDonagh and Smith9 (1958) on the transfer of infection between pigs held at abattoirs for extended periods. The significance of the healthy animal or fowl excreting salmonella is that during slaughter contamination of the surfaces of carcases with intestinal contents is unavoidable.
TABLE V Human volunteer experiments (percentages in parentheses)
HUMAN SALMONELLOSIS THE PERIOD examined is from 1940 to 1973, for which years human salmonellosis is adequately documented in the Annual Reports of Food Poisoning of the P.H.L.S.2 ’0 &dquo; Figure 1 shows the trends of human infections with S. typhi-murium and with serotypes other than S. typhi-murium during the period. In general three main trends can be distinguished. 1939-55. During this period human food and animal feed was rationed and infections were reduced to a minimum. As milk was regarded as a most important human food the greater part of imported animal feed was allocated to dairy cattle. Pig and poultry populations received only the amount necessary to maintain breeding herds and flocks. The fall in egg production was made up by the import of spray-dried egg from the U.S.A. and other countries for which contracts for production had been negotiated before the War. The control of meat supplies was effected by a reduction in the number of abattoirs from a pre-War figure of about 15,000 to 500 whose production was controlled. The restriction of cattle feed resulted in the slaughter of almost all the male calves produced by the dairy herd, in number 1 to 1.5 million annually. The concentration of animals at collecting centres and abattoirs during this period offered opportunity for the transfer of salmonella infection with consequent contamination of carcase meats with salmonellae from gut contents during slaughter. During this period, canned meats formed part of the meat ration and
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28 canned and
raw
meats were
commonly
delivered
together by retailers, affording opportunity of contaminormally eaten without further cooking, by carcase meats. In the period 1923-39 only fourteen salmonella nation of canned meats,
serotypes had been isolated from human infections in
and Wales. Spray-dried egg introduced another thirty-four serotypes which appeared in both human and pig populations as material unfit for human consumption was used to supplement supplies of animal feed. The import of spray-dried egg from the U.S.A. ceased with the abrupt ending of Lease-Lend in 1947, and imports of frozen liquid egg were obtained from ’soft currency’ arenas mainly within the Commonwealth. Some liquid egg was home-produced, mainly from cracked eggs at packing stations. Liquid egg introduced further serotypes from 1947 until 1964 when pasteurization of liquid egg became compulsory. Extensive surveys of liquid egg in the mid-1950s showed that Chinese liquid egg and egg products were heavily contaminated with S. paratyphi B and that homeproduced liquid egg was heavily contaminated with S. typhi-murium. The main vehicles through which these serotypes were conveyed to the population were sweetmeats and bakers’ confectionery, as liquid egg was used raw in the production of artificial creams. The ending of the rationing of human food and animal feed in 1953 led paradoxically to an immediate rise in human infection: the result of the distribution of food stocks accumulated by the Ministry of Food and of the return of abattoirs to private hands. The number of abattoirs increased in a relatively short period from 500 controlled abattoirs to about 5,000 private abattoirs where the shortage of experienced slaughtermen and meat inspectors was evident.
England
FIGURE 1. Incidents
of human
salmonella
infection England and Wales
After the hot summer of 1959 however, a general fall in infections with S. typhi-murium became apparent. This trend continued to 1965, after which year the annual incidence of S. typhi-murium infection became stabilized. This fall was the result of many factors of which the limitation of production of liquid egg to licensed plants, the introduction of pasteurization by the British Egg Marketing Board after its formation in 1957 and the growth of calf rearing which reduced to a minimum the number of day-old calves sent for slaughter are probably the most important. The marked increase in the number of infections with serotypes other than S. typhi-murium which occurred after the cessation of rationing may be attributed to the rapid reconstitution of the pig and poultry industries from the breeding stocks maintained during the period of rationing. With the import of animal and marine protein (meat and bone meals, fish meals) heavily contaminated with salmonella (notably Angolan sun-dried fish meal) many serotypes were introduced not only to England and Wales but to Europe at large. Once introduced many serotypes persisted, being recycled to animals through the conversion of inedible offals into animal feed. The most important factor in the increase of human infections due to other serotypes was the reconstitution of the poultry industry, both egg producing and broiler producing, which was remade on intensive lines in which a small number of specialist breeders supplied millions of day-old chicks to rearing farms. The cycle of transmission from the introduction of infection into a breeding flock has already been describedg and transmission of infection to man by raw egg products or by poultry meat can continue for many years without the necessity for continued introductions. By the end of the 1950s frozen eviscerated broiler
resulting
1942-73
3-year moving average.
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29 had replaced chilled uneviscerated poultry and had allowed expansion of the industry to proceed at so rapid a rate that by 1964, frozen poultry meat had become the cheapest flesh food available. Consumption of poultry meat increased so that by the 1970s, the annual consumption per head of poultry meat exceeded that of lamb and mutton and equalled consumption of pork. From 1963 onwards the import of fertile eggs for hatching and of day-old chicks was resumed to introduce desirable genes into native poultry breeding stocks. This led to the associated importation of salmonella serotypes, notably S. infantis, S. heidelberg, S. montevideo, S. indiana, and S. enteritidis, which became rapidly established in breeding flocks with egg transmission to offspring. Two serotypes, Salmonella unidentified 4, 12:d:-, and S. agona were introduced into poultry, pig and cattle herds through contaminated imported fish meals towards the end of the 1960s.
TABLE VI
carcases carcases
Human Salmonellosis Vehicles of infection. General and family outbreaks.
TABLE VII Human Salmonellosis Meat vehicles. General and family outbreaks.
&dquo;
VEHICLES OF INFECTION TABLE VI shows the foods involved in general and family outbreaks for which information was available. These outbreaks, 1,032 over the entire period, represent about 9 per cent of the 11,539 outbreaks reported. The trends of interest are the increasing proportion of outbreaks attributed to meat and milk, and the decreasing proportion attributed to sweetmeats which include bakers’ confectionery, and eggs. This latter trend can be attributed to the decrease in consumption of duck eggs which during food rationing were unrationed and the introduction of pasteurization for
TABLE VIII Human Salmonellosis. England and Wales Location of Outbreaks.
liquid
egg. The milk outbreaks were generally attributed to the consumption of raw milk which is currently supplied by about 6,000 producer retailers and represents about 3 per cent of milk consumption. Many of these outbreaks occurred in the families of milk producers where cows were infected with S. dublin or S. typhi-murium. The remainder were extensive outbreaks occurring in institutions, holiday camps and hotels supplied with raw milk. In a proportion of these latter outbreaks, symptomless excretion of the serotype responsible was demonstrated in the herds involved. Table VII shows general trends in the type of meats involved in general and family outbreaks. Two main trends are apparent: an increase in outbreaks attributed to poultry; a decrease in those attributable to made-up meats. During the period of food rationing and immediately afterwards made-up meats were involved in approximately 30 per cent of outbreaks. Readycooked meats (roast beef, pork, boiled ham) prepared centrally and distributed to retailers over wide areas have been increasingly identified as vehicles of infection. In the outbreaks recorded, undercooking or post-cooking contamination has been common. This problem results from the shrinkage of flesh meats on cooking, and a fine balance has to be struck empirically between adequate cooking and minimum shrinkage. Poultry outbreaks have been generally associated with spit-roasted poultry and turkey outbreaks associated with large (20-25 lb) ’banqueting’ birds. Most of these latter outbreaks have been associated with inadequate cooking, inadequate cooling, or postcooking contamination of sliced meats. Table VIII shows the trends in the locations where outbreaks have occurred. Throughout the period considered roughly 50 per cent of outbreaks of salmonellosis reported have occurred in hospitals.
Outbreaks
however,
are, occurring in hospitals andtoinstitutions likely to be brought attention more
more
rapidly and to be more thoroughly investigated and reported than outbreaks in other locations. Much the same consideration applies to canteen and institutional outbreaks, which share with hospitals a known population easily accessible for investigation of outbreaks. In hospitals, particularly children’s hospitals, maternity hospital nurseries, and geriatric hospitals and wards, outbreaks, not food-borne, often originate from the admission of an undiagnosed case of salmonellosis or symptomless excretor of salmonella, from whom infection is transmitted by direct or indirect contact. In some of such hospital outbreaks, infections have occurred for many weeks or even months. Experience suggests that about 50 per cent of hospital outbreaks fall into this category.
Hotel outbreaks occurred at more or less the same level until the period 1969/72, when outbreaks doubled. This increase can be associated with dinners and receptions at which the large ’banqueting’ birds previously mentioned were served. Table IX shows the change in rank order of the ten serotypes most frequently isolated from human infections over the period. Of the serotypes isolated in England and Wales up to 1939, three, S. typhi-murium, S. enteritidis, and S. stanley hold their original position. S. thompson, egg transmitted in laying flocks, ceased to be of major
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30
rationing in
TABLE IX
Salmonellosis.
England
1953. S.
brandenburg was introduced in the
same manner.
and Wales
S. virchow was associated with spit-roasted poultry since an extensive outbreak from this source in 1968. S. agona has been associated with meat, milk and poultry products since its introduction in imported fish meal.
Rank order of the top 10 serotypes
REFERENCES
1 SOJKA, W. J. and FIELD, H. I. (1970) "Salmonellosis in England and Wales 1958-1967." Veterinary Bulletin, 40, 515. 2 PHLS reports. "Food Poisoning in England and Wales. Annual reports 1958-1967." Monthly Bulletin of the Ministry of Health and the Public Health
Laboratory Service
1959-1967. Public
Health, London (1969) 83, 205.
3 Report (1964). "Salmonellae in abattoirs, butcher shops, and home-produced meat, and their relation to human infection." Journal
4
5
6
7
of Hygiene, 62,
283.
N. B. and EISELE, C. W. (1951a). "Experimental Human Salmonellosis. I." Journal of Infectious Diseases, 88, 278. McCULLOUGH, N. B. and EISELE, C. W. (1951b). "Experimental Human Salmonellosis. III ." Journal of Infectious Diseases, 89 , 209. McCULLOUGH, N. B. and EISELE, C. W. "Experimental Human Salmonellosis. IV." Journal of Infectious Diseases, 89, 259. SMITH, H. WILLIAMS (1960). "The effect of feeding pigs on food
McCuLLOUGH,
naturally contaminated with Salmonellae."Journal of Hygiene, 58,
381. R. F. and TUCKER, J. F. (1965). "The epizootology of Salmonella Menston infection of fowl and the effect of feeding poultry food artificially infected with salmonella." British Poultry Science, 6, 251. 9 McDONAGH, V. P. and SMITH, H. G. (1958). "The Significance of the Abattoir in Salmonella infection in Bradford." Journal of Hygiene, 56, 271. Reports (1970). "Food Poisoning and Salmonella infections in 10 England and Wales. 1968." Public Health, London, 84, 239. 11 Reports (1974). "Food Poisoning and Salmonella infections in . 225 England and Wales. 1969-1972." Public Health, London, 88,
8 GORDON,
importance after the introduction of pasteurization of liquid egg in 1964, though a small number of infections with this serotype still occur. S. meleagridis, S. oranienburg, S. montevideo, and S. anatum, were introduced by imported spray-dried hen egg during the period of rationing, and were later introduced to flocks and herds by imported protein constituents of animal feed after the cessation of
SALMONELLA INFECTIONS IN ANIMALS AND BIRDS
A. D. OSBORNE, M.R.C.V.S., D.V.S.M., M.R.C.PATH,
Senior Lecturer in
Veterinary Public Health, University of Bristol
the first identification of a specific orassociated with disease in pigs, which was the name Bacillus cholerae-suis by Salmon in 1885, the widespread implication of similar organisms with disease processes in animals of almost every species has been demonstrated. Although by no means absolute it is possible to make a distinction between those members of the group which are primarily involved with disease in a single host (e.g. Salmonella typhi in man S. abortus ovis in sheep, S. pullorum in poultry) and those which are associated with disease, or occasionally found as little more than commensals, in a wide variety of animal species (e.g. S. typhimurium, S.
INCE
ganism given
F.R.S.H.
newport).
It is the latter group with which this paper is concerned in the main, since the Zoonoses Order is obviously designed to improve the possibilities of control of spread of such agents. In consideration of hosts of such salmonella, those from which humans are most likely to derive infection must be our primary concern, but opportunity will be taken to indicate some of the less common possible sources of infection for man.
In considering diseases associated with infection by members of this large group of organisms, it is salutary to realize that the incidence of infection has decreased
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